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PMID: 25082815 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

CSF1/CSF1R blockade reprograms tumor-infiltrating macrophages and improves response to T-cell checkpoint immunotherapy in pancreatic cancer models.

Cancer research ·Vol. 74 ·No. 18 ·2014-09-15 ·Pages 5057-69

Zhu Y, Knolhoff BL, Meyer MA, Nywening TM, West BL, Luo J, Wang-Gillam A, Goedegebuure SP, Linehan DC, DeNardo DG

Abstract

Cancer immunotherapy generally offers limited clinical benefit without coordinated strategies to mitigate the immunosuppressive nature of the tumor microenvironment. Critical drivers of immune escape in the tumor microenvironment include tumor-associated macrophages and myeloid-derived suppressor cells, which not only mediate immune suppression, but also promote metastatic dissemination and impart resistance to cytotoxic therapies. Thus, strategies to ablate the effects of these myeloid cell populations may offer great therapeutic potential. In this report, we demonstrate in a mouse model of pancreatic ductal adenocarcinoma (PDAC) that inhibiting signaling by the myeloid growth factor receptor CSF1R can functionally reprogram macrophage responses that enhance antigen presentation and productive antitumor T-cell responses. Investigations of this response revealed that CSF1R blockade also upregulated T-cell checkpoint molecules, including PDL1 and CTLA4, thereby restraining beneficial therapeutic effects. We found that PD1 and CTLA4 antagonists showed limited efficacy as single agents to restrain PDAC growth, but that combining these agents with CSF1R blockade potently elicited tumor regressions, even in larger established tumors. Taken together, our findings provide a rationale to reprogram immunosuppressive myeloid cell populations in the tumor microenvironment under conditions that can significantly empower the therapeutic effects of checkpoint-based immunotherapeutics.

MeSH Terms
Adenocarcinoma/immunology,pathology Animals Carcinoma, Pancreatic Ductal/immunology,pathology,therapy Cohort Studies Deoxycytidine/analogs & derivatives,pharmacology Female Humans Immunotherapy/methods Lectins, C-Type/biosynthesis,immunology Macrophage Colony-Stimulating Factor/antagonists & inhibitors,biosynthesis,immunology Macrophages/immunology Mannose Receptor Mannose-Binding Lectins/biosynthesis,immunology Mice Mice, Inbred C57BL Pancreatic Neoplasms/immunology,pathology,therapy Random Allocation Receptor, Macrophage Colony-Stimulating Factor/antagonists & inhibitors,immunology Receptors, Cell Surface/biosynthesis,immunology Signal Transduction T-Lymphocytes/immunology Tissue Array Analysis Tumor Microenvironment
Chemicals
Lectins, C-Type Mannose Receptor Mannose-Binding Lectins Receptors, Cell Surface Deoxycytidine Macrophage Colony-Stimulating Factor gemcitabine Receptor, Macrophage Colony-Stimulating Factor
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zhu Yu
Department of Medicine, Washington University School of Medicine, St Louis, Missouri. BRIGHT Institute, Washington University School of Medicine, St Louis, Missouri.
Knolhoff Brett L
Department of Medicine, Washington University School of Medicine, St Louis, Missouri. BRIGHT Institute, Washington University School of Medicine, St Louis, Missouri.
Meyer Melissa A
Department of Medicine, Washington University School of Medicine, St Louis, Missouri. BRIGHT Institute, Washington University School of Medicine, St Louis, Missouri.
Nywening Timothy M
Department of Surgery, Washington University School of Medicine, St Louis, Missouri. Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri.
West Brian L
Plexxikon Inc., Berkeley, California.
Luo Jingqin
Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri. Division of Biostatistics, Washington University School of Medicine, St Louis, Missouri.
Wang-Gillam Andrea
Department of Medicine, Washington University School of Medicine, St Louis, Missouri.
Goedegebuure S Peter
Department of Surgery, Washington University School of Medicine, St Louis, Missouri. Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri.
Linehan David C
Department of Surgery, Washington University School of Medicine, St Louis, Missouri. Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri.
DeNardo David G
Department of Medicine, Washington University School of Medicine, St Louis, Missouri. BRIGHT Institute, Washington University School of Medicine, St Louis, Missouri. Siteman Cancer Center, Washington University School of Medicine, St Louis, Missouri. Department of Pathology and Immunology, Washington University School of Medicine, St Louis, Missouri. ddenardo@dom.wustl.edu.
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Article Info
Journal
Cancer research
Abbr.
Cancer Res
ISSN
1538-7445
Published
2014-09-15
Epub
2014-00-31
Pages
5057-69
Language
English
Region
United States
NLM ID
2984705R
PMCID
PMC4182950
Subset
IM
Grants
NCI NIH HHS · T32 CA113275 · United States
NCATS NIH HHS · KL2TR000450 · United States
NCI NIH HHS · T32 CA 009621 · United States
NCI NIH HHS · T32 CA009621 · United States
NCI NIH HHS · R01 CA177670-01 · United States
NCI NIH HHS · R01 CA168863-01 · United States
NCI NIH HHS · P30 CA091842 · United States
NCI NIH HHS · R21 CA182701 · United States
NCATS NIH HHS · KL2 TR000450 · United States
NCRR NIH HHS · UL1RR024992 · United States
NCRR NIH HHS · UL1 RR024992 · United States
NCI NIH HHS · P30 CA91842 · United States
NCI NIH HHS · R01 CA177670 · United States
NCATS NIH HHS · UL1 TR000448 · United States
NCRR NIH HHS · KL2 RR024994 · United States
NCI NIH HHS · R01 CA168863 · United States
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